Avian cold adaptation is hallmarked by innovative strategies of both heat conservation and thermogenesis. While minimizing heat loss can reduce the thermogenic demands of body temperature maintenance, it cannot eliminate the requirement for thermogenesis. Shivering and non-shivering thermogenesis (NST) are the two synergistic mechanisms contributing to endothermy. Birds are of particular interest in studies of NST as they lack brown adipose tissue (BAT), the major organ of NST in mammals. Critical analysis of the existing literature on avian strategies of cold adaptation suggests that skeletal muscle is the principal site of NST. Despite recent progress, isolating the mechanisms involved in avian muscle NST has been difficult as shivering and NST co-exist with its primary locomotory function. Herein, we re-evaluate various proposed molecular bases of avian skeletal muscle NST. Experimental evidence suggests that sarco(endo)plasmic reticulum Ca2+ -ATPase (SERCA) and ryanodine receptor 1 (RyR1) are key in avian muscle NST, through their mediation of futile Ca2+ cycling and thermogenesis. More recent studies have shown that SERCA regulation by sarcolipin (SLN) facilitates muscle NST in mammals; however, its role in birds is unclear. Ca2+ signalling in the muscle seems to be common to contraction, shivering and NST, but elucidating its roles will require more precise measurement of local Ca2+ levels inside avian myofibres. The endocrine control of avian muscle NST is still poorly defined. A better understanding of the mechanistic details of avian muscle NST will provide insights into the roles of these processes in regulatory thermogenesis, which could further inform our understanding of the evolution of endothermy among vertebrates.